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J AIDS Clin Res. Author manuscript; available in PMC 2017 September 07. Published in final edited form as: J AIDS Clin Res. 2017 July ; 8(7): . doi:10.4172/2155-6113.1000708.

Magnetic Resonance Imaging Evidence for Human Immunodeficiency Virus Effects on Central Auditory Processing: A Review Yi Zhan1, Jay C Buckey2,*, Abigail M Fellows2, and Yuxin Shi1 1Department

of Radiology, Shanghai Public Health Clinic Center, Fudan University, Shanghai,

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China 2Geisel

School of Medicine at Dartmouth, Hanover, NH, USA

Abstract

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New research suggests that individuals with human immunodeficiency virus (HIV) have central auditory processing deficits. To review the evidence for HIV affecting parts of the central nervous system involved in central auditory processing, we performed a systematic review of the literature. The objective was to determine whether existing studies show evidence for damage to structures associated with central auditory pathways in HIV. We searched PubMed for papers that used structural magnetic resonance imaging (MRI), diffusion tensor imaging, magnetic resonance spectroscopy or functional MRI in individuals infected with HIV. The review showed that HIV affects several areas involved in central auditory processing particularly the thalamus, internal capsule and temporal cortex. These findings support the idea that HIV can affect central auditory pathways and support the potential use of central auditory tests as a way to assess central nervous system effects of HIV.

Keywords HIV; HAND; APD; MRI

Introduction

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Although otologic problems were common early in the HIV epidemic [1], recent studies have shown either small or no differences in peripheral hearing ability (audiometry) between HIV-infected and HIV-uninfected individuals [2–4]. Bankaitis and Keith provided a casereport of an HIV+ individual with normal peripheral auditory function who also had difficulty with speech perception, particularly with competing sentences [5]. This may indicate that central auditory system may be involved in HIV infection. Recent research found that HIV positive individuals have significant differences in word recognition scores [6] and abnormalities in auditory evoked potentials consistent with a higher rate of central

This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. * Corresponding author: Jay C Buckey, M.D., Geisel School of Medicine at Dartmouth, Hanover, NH, USA; Tel: 603-650-6012; [email protected].

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auditory defects [5,7,8], compared to HIV-negative subjects, showing central auditory processing deficits (CAPD) may exist in HIV infected patients. Central auditory processing is a cognitively demanding task, therefore the findings of central auditory processing deficits may correlate with HIV-related central nervous system effects, such as HIV-associated neurocognitive disorder (HAND) [9,10]. Even with active antiretroviral therapy, HIV+ individuals continue to develop neurocognitive deficits [11] and HAND. MRI and pathological studies show evidence of glial activation and inflammation even without documented cognitive deficits [12–14]. Central auditory processing deficits in HIV+ people may have relationship with HAND or may serve as an independent sign of HIV effects on the central nervous system (CNS). There have been many MRI studies of the brain in individuals with HIV. To date, however, there has not been any direct evidence that HIV affects pathways associated with central auditory processing.

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The auditory pathways in the brain include sites in the brainstem (cochlear nucleus), the midbrain (inferior colliculus), the thalamus (medial geniculate body), the internal capsule, the temporal cortex, and the corpus callosum. Also, a recent study using diffusion tensor imaging (DTI) suggested that the sites in the prefrontal cortex and anterior cingulate may also be involved in auditory processing [15]. The objective of this review was to assess the evidence in existing MR studies for HIV affecting the parts of the central nervous system involved in central auditory processing.

Methods Author Manuscript

We searched PubMed over the last 10 years looking for articles with the search terms MRI, HIV and brain (MRI and (HIV or AIDS) and brain)) published in English. This resulted in 775 articles. Of those, only articles directly concerned with measuring biochemical, anatomical or functional changes due to HIV were included. For example, studies examining central nervous system lymphoma, neurosyphilis or other conditions were excluded.

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We focused on articles that specifically mentioned anatomic structures directly involved in central auditory processing (e.g. inferior colliculus (midbrain), medial geniculate body (thalamus), internal capsule (basal ganglia region), temporal cortex, and corpus callosum (particularly the splenium)). The articles were reviewed to assess whether the anatomic structures mentioned were reasonable to include as relevant to auditory processing. For example, multiple studies examined the basal ganglia. In some studies, procedures were used to measure particular regions within the basal ganglia (e.g. caudate or putamen). These studies were not included in the analysis since these nuclei are not universally agreed to be involved in central auditory processing. Other studies, however, selected the basal ganglia region as a region of interest. In this case, the study would be included since the region of interest would include, not just the nuclei in the basal ganglia, but also the white matter in the internal and external capsule around the basal ganglia. This resulted in a total of 171 articles: 59 for volumetric measurement, 43 for magnetic resonance spectroscopy (MRS), 38 for diffusion tensor imaging (DTI), 42 for functional magnetic resonance imaging (fMRI), 9 review articles, and 19 animal trials. These papers

J AIDS Clin Res. Author manuscript; available in PMC 2017 September 07.

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were further screened to remove articles that: (a) did not have a comparison to a control group, or were a longitudinal study within an HIV+ group, or (b) were focused on particular subsets of HIV+ people (like those with alcoholism, or taking methamphetamines). Only fMRI resting state articles were included since no articles that used an auditory stimulus were found. Figure 1 summarizes the procedure used to select the articles. The final set included 29 articles, 20 focused on volumetric measurement, 1 resting state fMRI study, 5 DTI studies and 4 MRS studies.

Results

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Compared with HIV− controls, patients with HIV have gray matter atrophy, diffuse white matter abnormalities, differences in resting state activation on fMRI, and changes in neuronal metabolites in various brain regions. Changes in brain areas relevant to central auditory processing are summarized in Table 1. Tissue loss and white matter abnormalities from T1 and T2 imaging T1-weighted imaging by high resolution MR in a 1.5T or 3T field, can be used to measure the volume of brain regions. Aylward et al. [16] concluded that HIV infection causes generalized brain atrophy and also selective basal ganglia atrophy, consistent with the characterization of HIV dementia as subcortical. The internal capsule, however, was excluded from their analysis. However, some researchers studied 94 HIV+ individuals and assessed the severity of white matter abnormalities in the basal ganglia region. Thirty-two percent of the subjects (30/94) had detectable white matter abnormalities in this region.

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Heaps et al. [17] found significantly smaller brain volumes in their HIV+ HAND+ group compared to the HIV− group. There was a tendency for thalamic volume to be smaller in the HIV+/HAND+ group compared to the HIV− group (p=0.06). When the analysis was done categorizing the subjects by functional impairment, thalamic volume was significantly smaller (p=0.02) in those HIV+ indiviudals with functional impairment compared to HIV− controls. Wade et al. using surface-based shape analysis in an older HIV+ cohort (mean age 65), also showed significantly smaller thalamic volume in HIV+ subjects compared to HIV− controls. Since the thalamus contains the medial geniculate body, this finding may be relevant for auditory processing. The corpus callosum may also be affected. Wade et al. [18] showed that HIV+ individuals had a significantly smaller callosum compared to HIV− participants (p

Magnetic Resonance Imaging Evidence for Human Immunodeficiency Virus Effects on Central Auditory Processing: A Review.

New research suggests that individuals with human immunodeficiency virus (HIV) have central auditory processing deficits. To review the evidence for H...
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